Freshwater Biology (2015) 60, 2226–2247 doi:10.1111/fwb.12650 Ecological sensitivity of marl lakes to nutrient enrichment: evidence from Hawes Water, UK † ‡ § EMMA WIIK* , HELEN BENNION*, CARL D. SAYER*, THOMAS A. DAVIDSON , ¶ †† SUZANNE MCGOWAN **, IAN R. PATMORE* AND STEWART J. CLARKE *Environmental Change Research Centre, Department of Geography, University College London, London, U.K. † Institute of Environmental Change and Society, Research and Innovation Centre, University of Regina, Regina, SK Canada ‡ Lake Group, Department of Bioscience, Aarhus University, Silkeborg, Denmark § Section for Ecoinformatics and Biodiversity, Department of Bioscience, Aarhus University, Aarhus, Denmark ¶ School of Geography, University of Nottingham, Nottingham, U.K. **School of Geography, University of Nottingham Malaysia Campus Jalan Broga, Selangor Darul Ehsan, Malaysia †† The National Trust, Bury St Edmunds, Suffolk, U.K. SUMMARY 1. Highly calcareous (marl) lakes are infrequent but important freshwater ecosystems, protected under the EU Habitats and Species Directive. Chara lakes have been considered resistant to eutrophication owing to the self-stabilising properties of charophyte meadows. However, the opposite is suggested by the large-scale biodiversity declines in marl lake taxa in Europe, and evidence of charophyte sensitivity to eutrophication. We combined contemporary, palaeolimnological and archival methods to investigate the eutrophication of Hawes Water, a shallow marl lake in north-west England (U.K.). 2. Changes in aquatic macrophyte and invertebrate communities were reconstructed through the analysis of historical macrophyte surveys and sedimentary plant and animal macrofossils in two dated sediment cores from the littoral and deep zones of the lake. In addition, chlorophyll and caro- tenoid pigments were analysed to track changes in primary production from benthic and pelagic areas. Substantial changes in macrophyte communities were detected over centennial timescales, sug- gesting high ecosystem sensitivity considering the presently moderate phosphorus concentrations in À Hawes Water (mean annual total phosphorus 20 lgL 1). 3. Two apparent periods of threshold-like change were identified from the sediment record: (i) changes in cyanobacteria (aphanizophyll + myxoxanthophyll to canthaxanthin + zeaxanthin) and potentially in nutrient stoichiometry, reductions in the maximum macrophyte colonisation depth and water clarity, reduced charophyte and Potamogeton diversity, and increases in Nymphaeaceae; and (ii) severe reduc- tions in light availability inferred from subdecadal doubling in phytoplankton abundance, substantial increases in Daphnia abundance and the extinction of charophytes from higher water depths. 4. Further, change in both the littoral and deeper water has confined key marl lake taxa to smaller niches. In the littoral, increasing siltation and reed and Nymphaeaceae densities caused extinction of Littorella uniflora in the early 1900s and have reduced the evenness of Characeae with suspected imminent extinction of two highly localised Chara spp. In the deeper water, upslope creep of maxi- mum colonisation depth has reduced habitat for intermediate-depth marl lake taxa leading to the loss of four Potamogeton and one Chara species, and replacement of these taxa by Nuphar lutea. 5. The large changes in macrophyte community composition and increased incidences of turbid water have reduced the distinctive and valued marl lake features of Hawes Water, indicating that marl lakes can, as a habitat type, be highly sensitive to eutrophication. The persistence of abundant generalist macrophyte species at considerable water depth may be a feature of high-alkalinity lakes in clearwater, macrophyte-dominated states, but is a distinct eutrophication response in marl lakes rather than an indication of resistance to eutrophication. Correspondence: Emma Wiik, Laboratory Building, Department of Biology, University of Regina, 3737 Wascana Parkway, Regina, Saskatche- wan, S4S0A2 Canada. E-mail: [email protected] 2226 © 2015 The Authors Freshwater Biology Published by John Wiley & Sons Ltd. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. Evidence for eutrophication in a low-nutrient English marl lake 2227 Keywords: eutrophication, macrophytes, marl lakes, palaeolimnology, pigments capacity, following the predictions of regime shift and Introduction alternative stable state hypotheses (Scheffer et al., 1993; Marl lakes are calcite-depositing, high-alkalinity lakes, Scheffer & van Nes, 2007; Blindow, Hargeby & Hilt, globally distributed in areas of carbonate geology. They 2014). Despite prevailing theory suggesting resistance of are distinct from other lake types owing to their particu- Chara lakes to eutrophication, empirical evidence sug- larly clear, blue-green water, white calcareous sedi- gests that the macrophyte communities of marl lakes ments, and remarkably high macrophyte colonisation may actually be highly sensitive to nutrient enrichment depths (>10 m). Further, the macrophyte community (Wiik et al., 2013). For example, substantial declines in composition of marl lakes, consisting of a diversity of charophyte stands have been associated with total phos- À charophyte and Potamogeton species (Palmer, Bell & But- phorus (TP) exceeding only 7 lgL 1 (Free et al., 2007) À1 terfield, 1992; Duigan, Kovach & Palmer, 2007), is recog- and nitrate-N (NO3-N) exceeding 2 mg L (Lambert & nised in the European Union Habitats and Species Davy, 2011). Further, shifts between clear and turbid Directive (EC-DG ENV, 2007), awarding marl lakes spe- conditions have occurred at relatively low TP concentra- À cial protection as a habitat. However, wherever marl tions (from c.20to70lgL 1, respectively) (Hargeby, lakes are found, their characteristic macrophyte species Blindow & Andersson, 2007). However, owing to the are declining, while taxa tolerant of human impact, espe- high biomass attained by charophytes, substantial cially eutrophication, are becoming more abundant amounts of nutrients can be locked into the benthos (Sand-Jensen et al., 2000; Kłosowski, Tomaszewicz & (Pełechaty et al., 2013; Pukacz, Pełechaty & Frankowski, Tomaszewicz, 2006; Baastrup-Spohr et al., 2013). Conse- 2014), detracting from the relevance of pelagic measures quently, concerns over the ecological quality of marl of eutrophication (e.g. TP, chlorophyll a). Substantial lakes have been raised (Blazen cic et al., 2006; Pentecost, ecological degradation in the benthos may occur prior 2009; Azzella et al., 2013). Eutrophication effects, such as to any increases in planktonic production. increased phytoplankton production, associated reduced It seems likely that the overwhelming majority of marl water transparency, as well as low sediment cohesion lakes have been impacted by human activity (Jeppesen, (Egertson, Kopaska & Downing, 2004; Schutten, Dainty Jensen & Søndergaard, 2002; James et al., 2005; Bennion & Davy, 2005) can be particularly damaging to marl et al., 2011), while minimally impacted sites tend to lie lakes because they restrict macrophyte colonisation in inaccessible, less researched areas (Blazen cic et al., depth and induce an upslope retreat of charophytes and 2006), leaving knowledge gaps at the early stages of Potamogetonaceae. The retreat in turn compresses plant eutrophication where more subtle, yet significant, com- communities into a much narrower depth range and munity responses may occur. Palaeolimnological analy- thereby reduces species diversity (Middelboe & Mark- ses can provide a means to estimate pristine conditions, ager, 1997; Penning et al., 2008). and also detect changes in marl lakes over the decadal– Traditionally, marl lakes have been considered resili- centennial timescales relevant to long-term eutrophica- ent to eutrophication owing to the precipitation of phos- tion impacts, providing potentially more ecologically phorus with calcite (coprecipitation) (Otsuki & Wetzel, meaningful information than extrapolation from extant 1972; House, 1990; Robertson et al., 2007). Calcite deposi- analogue sites (Osborne & Moss, 1977; Moss, 1979; Sayer tion occurs predominantly in summer when photosyn- et al., 2010a). thesis increases pH and when water temperatures are Our study aimed to establish the early ecological relatively high, both of which induce carbonate oversat- changes that occur in marl lakes as a response to minor uration (Brunskill, 1969; Murphy, Hall & Yesaki, 1983). nutrient enrichment. We applied a combination of his- Therefore, macrophytes (especially charophytes) can pre- torical investigations, limnological monitoring (2009– vent phytoplankton dominance and maintain clearwater 2010) and palaeolimnology to Hawes Water (Lancashire, conditions via recycling of sediment-bound nutrients, U.K.) which currently has moderate limnetic phosphorus and inducing coprecipitation in the water column. The and chlorophyll a concentrations. Hawes Water has pre- strong negative feedback exerted by charophytes on viously been described as the ‘best example of a lowland external nutrient loading may lead to threshold marl lake in England’ (Bennion et al., 2009) and is responses once the latter exceeds their buffering classed as oligotrophic (Skelcher, 2014). We hypothesised © 2015 The Authors Freshwater Biology Published by John Wiley & Sons Ltd., Freshwater Biology, 60, 2226–2247 2228 E. Wiik